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Molecular and Cellular Biology, October 2009, p. 5632-5638, Vol. 29, No. 20
0270-7306/09/$08.00+0     doi:10.1128/MCB.00664-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Coupled RNA Processing and Transcription of Intergenic Primary MicroRNAs{triangledown} ,{dagger}

Monica Ballarino,1,{ddagger} Francesca Pagano,1,{ddagger} Erika Girardi,1 Mariangela Morlando,1,2 Davide Cacchiarelli,1 Marcella Marchioni,1 Nicholas J. Proudfoot,2 and Irene Bozzoni1*

Institute Pasteur Cenci-Bolognetti, Department of Genetics and Molecular Biology and IBPM, Sapienza University of Rome, P.le A. Moro 5, 00185 Rome, Italy,1 Sir William Dunn School of Pathology, University of Oxford, South Parks Rd., Oxford OX1 3RE, United Kingdom2

Received 22 May 2009/ Returned for modification 26 June 2009/ Accepted 3 August 2009

The first step in microRNA (miRNA) biogenesis occurs in the nucleus and is mediated by the Microprocessor complex containing the RNase III-like enzyme Drosha and its cofactor DGCR8. Here we show that the 5'->3' exonuclease Xrn2 associates with independently transcribed miRNAs and, in combination with Drosha processing, attenuates transcription in downstream regions. We suggest that, after Drosha cleavage, a torpedo-like mechanism acts on nascent long precursor miRNAs, whereby Xrn2 exonuclease degrades the RNA polymerase II-associated transcripts inducing its release from the template. While involved in primary transcript termination, this attenuation effect does not restrict clustered miRNA expression, which, in the majority of cases, is separated by short spacers. We also show that transcripts originating from a miRNA promoter are retained on the chromatin template and are more efficiently processed than those produced from mRNA or snRNA Pol II-dependent promoters. These data imply that coupling between transcription and processing promotes efficient expression of independently transcribed miRNAs.

* Corresponding author. Mailing address: University of Rome La Sapienza, P.le A. Moro 5, 00185 Rome, Italy. Phone: 390649912202. Fax: 390649912500. E-mail: irene.bozzoni{at}uniroma1.it

{triangledown} Published ahead of print on 10 August 2009.

{dagger} Supplemental material for this article may be found at http://mcb.asm.org/.

{ddagger} M. Ballarino and F. Pagano contributed equally to this study.

Molecular and Cellular Biology, October 2009, p. 5632-5638, Vol. 29, No. 20
0270-7306/09/$08.00+0     doi:10.1128/MCB.00664-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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